Phosphatidylinositol-3,4,5-trisphosphate (Ptdlns-3,4,5-P3)/Tec kinase-dependent calcium signaling pathway: A target for SHIP-mediated inhibitory signals

EMBO Journal

Volumn 17, Issue 7, 1998, Pages 1961-1972

  Scharenberg, Andrew M ^a   El Hillal, Ousama ^a   Fruman, David A ^a   Beitz, Laurie O ^a   Li, Zuomei ^a,b   Lin, Siqi ^a   Gout, Ivan ^a,c,d   Cantley, Lewis C ^a   Rawlings, David J ^a,b   Kinet, Jean Pierre ^a  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c LUDWIG INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^d INSTITUTE OF MOLECULAR BIOLOGY AND GENETICS   (Ukraine)

Author keywords

B cells; Inositol trisphosphate; Phospholipase C; Receptor; Tyrosine kinases

Indexed keywords

CALCIUM; CELL SURFACE RECEPTOR; PLECKSTRIN; POLYPHOSPHOINOSITIDE; PROTEIN TYROSINE KINASE;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CALCIUM TRANSPORT; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; BLOOD PROTEINS; CALCIUM; CELL LINE, TRANSFORMED; ENZYME ACTIVATION; ENZYME INHIBITORS; FIBROBLASTS; INOSITOL PHOSPHATES; ISOENZYMES; MUTATION; PHOSPHATIDYLINOSITOL PHOSPHATES; PHOSPHOLIPASE C; PHOSPHOLIPASE C GAMMA; PHOSPHOPROTEINS; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; RATS; RECEPTORS, ANTIGEN, B-CELL; RECEPTORS, IGG; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; TYROSINE;

ANIMALIA;

EID: 0032055484     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.7.1961     Document Type: Article

References (61)

1. Afar, D.E.H., Park, H., Howell, B.W., Rawlings, D.J., Cooper, J., and Witte, O.N. (1996) Regulation of Btk by Src family tyrosine kinases. Mol. Cell. Biol., 16, 3465-3471.
2. Alessi, D.R., James, S.R., Downes, C.P., Holmes, A.B., Gaffney, P.R., Reese, C.B. and Cohen, P. (1997) Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Bα. Curr. Biol., 7, 261-269.
3. Amigorena, S. et al. (1992) Cytoplasmic domain heterogeneity and functions of IgG Fc receptors in B lymphocytes. Science. 256, 1808-1812.
4. Andreotti, A.H., Bunnell, S.C., Feng, S., Berg, L.J. and Schreiber, S.L. (1997) Regulatory intramolecular association in a tyrosine kinase of the Tec family. Nature, 385, 93-97.
5. Auger, K.R., Serunian, L.A., Soltoff, S.P., Libby, P. and Cantley, L.C. (1989) PDGF-dependent tyrosine phosphorylation stimulates production of novel polyphosphoinositides in intact cells. Cell, 57, 167-175.
6. Bijsterbosch, M.K. and Klaus, G.G.B. (1985) Crosslinking of surface immunoglobulin and Fc receptors on B lymphocytes inhibits stimulation of inositol phospholipid breakdown via the antigen receptors. J. Exp. Med., 162, 1825-1836.
7. Bunnell, S.C., Henry, P.A., Kolluri, R., Kirchhausen, T., Rickles, R.J. and Berg, L.J. (1996) Identification of Itk/Tsk Src homology 3 domain ligands. J. Biol. Chem., 271, 25646-25656.
8. Carpenter, C.L, and Cantley, L.C. (1996) Phosphoinositide kinases. Curr. Opin. Cell Biol., 8, 153-158.
9. Conley, M.E. and Rohrer, J. (1995) The spectrum of mutations in Btk that cause X-linked agammaglobulinemia. Clin. Immunol. Immunopathol., 76, S192-S197.
10. Cory, G.O., Lovering, R.C., Hinshelwood, S., MacCarthy-Morrogh, L., Levinsky, R.J. and Kinnon, C. (1995) The protein product of the c-cbl protooncogene is phosphorylated after B cell receptor stimulation and binds the SH3 domain of Bruton's tyrosine kinase. J. Exp. Med., 182. 611-615.
11. Desiderio, S. and Siliciano, J.D. (1994) The Itk/Btk/Tec family of protein-tyrosine kinases. Chem. Immunol., 59, 191-210.
12. Earl, P.L., Cooper, N. and Moss, B. (1987) Expression of Proteins in Mammalian Cells Using Recombinant Vaccinia Viruses. Green Publishing and Wiley-Interscience, New York.
13. Falasca, M., Logan, S.K., Lehto, V.P., Baccante, G., Lemmon, M.A. and Schlessinger, J. (1998) Activation of phospholipase Cγ γby PI 3-kinase-induced PH domain-mediated membrane targeting. EMBO J., 17, 414-422.
14. 2+ following B-cell receptor activation. EMBO J., 17, 1973-1985.
15. Franke, T.F., Yang, S.I., Chan, T.O., Datta, K., Kazlauskas, A., Morrison, D.K., Kaplan, D.R. and Tsichlis, P.N. (1995) The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell, 81, 727-736.
16. Franke, T.F., Kaplan, D.R., Cantley, L.C. and Toker, A. (1997) Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3, 4-biphosphate. Science, 275, 665-668.
17. Fukuda, M., Kojima, T., Kabayama, H. and Mikoshiba, K. (1996) Mutation of the pleckstrin homology domain of Bruton's tyrosine kinase in immunodeficiency impaired inositol 1, 3, 4, 5-tetrakisphosphate binding capacity. J. Biol. Chem., 271, 30303-30306.
18. Gold, M.R. and Aebersold, R. (1994) Both phosphatidylinositol 3-kinase and phosphatidylinositol 4-kinase products are increased by antigen receptor signaling in B cells. J. Immunol., 152, 42-50.
19. Gold, M.R., Duronio, V., Saxena, S.P., Schrader, J.W. and Aebersold, R. (1994) Multiple cytokines activate phosphatidylinositol 3-kinase in hemopoietic cells. Association of the enzyme with various tyrosine-phosphorylated proteins. J. Biol. Chem., 269, 5403-5412.
20. Gupta, N., Scharenberg, A.M., Burshtyn, D.N., Wagtmann, N., Lioubin, M.N., Rohrschneider, L.R., Kinet, J.P. and Long, E.O. (1997) Negative signaling pathways of the killer cell inhibitory receptor and Fc gamma RIIb1 require distinct phosphatases. J. Exp. Med., 186, 473-478.
21. Hiles, I.D. et al. (1992) Phosphatidylinositol 3-kinase: structure and expression of the 110 kDa catalytic subunit. Cell, 70, 419-429.
22. Hippen, K.L., Buhl, A.M., Ambrosio, D.D., Nakamura, K., Persin, C. and Cambier, J.C. (1997) FcγRIIB1 inhibition of phosphoinositide hydrolysis and Ca mobilization is integrated by CD19 dephosphorylation. Immunity, 7, 49-58.
23. Hu, Q., Klippel, A., Muslin, A.J., Fantl, W.J. and Williams, L.T. (1995) Ras-dependent induction of cellular responses by constitutively activated phosphatidylinositol 3-kinase. Science, 268, 100-102.
24. Kawakami, Y., Yao, L., Tashiro, M., Gibson, S., Mills, G.B. and Kawakami, T. (1995) Activation and interaction with protein kinase C of a cytoplasmic tyrosine kinase, Itk/Tsk/Emt, on FcεRI cross-linking on mast cells. J. Immunol., 155, 3556-3562.
25. Kawakami, Y. et al. (1997) Bruton's tyrosine kinase regulates apoptosis and JNK/SAPK kinase activity. Proc. Natl Acad. Sci. USA, 94, 3938-3942.
26. Kiener, P.A., Lioubin, M.N., Rohrschneider, L.R., Ledbetter, J.A., Nadler, S.G. and Diegel, M.L. (1997) Co-ligation of the antigen and Fc receptors gives rise to the selective modulation of intracellular signaling in B cells. Regulation of the association of phosphatidylinositol-3 kinase and inositol 5'-phosphatase with the antigen-receptor complex. J. Biol. Chem., 272, 3838-3844.
27. Klarlund, K.J., Guilherme, A., Holik, J.J., Virbasius, J.V., Chawla, A. and Czech, M.P. (1997) Signaling by phosphoinositide-3, 4, 5-trisphosphate through proteins containing pleckstrin and Sec7 homology domains. Science, 275, 1927-1930.
28. Klippel, A., Reinhard, C., Kavanaugh, W.M., Apell, G., EscobedoM.A. and Williams, L.T. (1996) Membrane localization of phosphatidylinositol 3-kinase is sufficient to activate multiple signal-transducing kinase pathways. Mol. Cell. Biol., 16, 4117-4127.
29. Klippel, A., Kavanaugh, W.M., Pot, D. and Williams, L.T. (1997) A specific product of phosphatidylinositol 3-kinase directly activates the protein kinase Akt through its pleckstrin homology domain. Mol. Cell. Biol., 17, 338-344.
30. Law, C.L., Chandran, K.A., Sidorenko, S.P. and Clark, E.E. (1996) Phospholipase C-γl interacts with conserved phosphotyrosyl residues in the linker region of Syk and is a substrate for Syk. Mol. Cell. Biol., 16, 1305-1315.
31. Li, Z., Wahl, M.I., Eguinoa, A., Stephens, L.R., Hawkins, P.T. and Witte, O.N. (1997) Phosphatidylinositol 3-kinase-γ activates Bruton's tyrosine kinase in concert with Src family kinases. Proc. Natl Acad. Sci. USA, 94, 13820-13825.
32. Machide, M., Mano, H. and Todokoro, K. (1995) Interleukin 3 and erythropoietin induce association of Vav with Tec kinase through Tec homology domain. Oncogene, 11, 619-625.
33. Mahajan, S., Fargnoli, J., Burkhardt, A.L., Kut, S.A., Saouaf, S.J. and Bolen, J.B. (1995) Src family protein tyrosine kinases induce autoactivation of Bruton's tyrosine kinase. Mol. Cell. Biol., 15, 5304-5311.
34. Muta, T., Kurosaki, T., Misulovin, Z., Sanchez, M., Nussenzweig, M.C. and Ravetch, J.V. (1994) A 13-amino-acid motif in the cytoplasmic domain of FcγRIIB modulates B-cell receptor signalling. Nature, 368, 70-73.
35. Okada, T., Hazeki, O., Ui, M. and Katada, T. (1996) Synergistic activation of PtdIns 3-kinase by tyrosine-phosphorylated peptide and βγ-subunits of GTP-binding proteins. Biochem. J., 317, 475-480.
36. Ono, M., Bolland, S., Tempst, P. and Ravetch, J.V. (1996) Role of the inositol phosphatase SHIP in negative regulation of the immune system by the receptor FcγRIIB. Nature, 383, 263-266.
37. Ono, M., Okada, H., Bolland, S., Yanagi, S., Kurosaki, T. and Ravetch, J.B. (1997) Deletion of SHIP-1 reveals two distinct pathways for inhibitory signaling. Cell, 90, 293-301.
38. Park, H., Wahl, M.I., Afar, D.E., Turck, C.W., Rawlings, D.J., Tam, C., Scharenberg, A.M., Kinet, J.-P. and Witte, O.N. (1996) Regulation of Btk function by a major autophosphorylation site within the SH3 domain. Immunity, 4, 515-525.
39. Pike, L.J. and Casey, L. (1996) Localization and turnover of phosphatidylinositol 4, 5-bisphosphate in caveolin-enriched membrane domains. J. Biol. Chem., 271, 26453-26456.
40. 3 interacts with SH2 domains and modulates PI 3-kinase association with tyrosine-phosphorylated proteins. Cell, 83, 821-830.
41. Rameh, L.E. et al (1997) A comparative analysis of the phosphoinositide binding specificity of pleckstrin homology domains. J. Biol. Chem., 272, 22059-22066.
42. Rawlings, D.J. and Witte, O.N. (1995) The Btk subfamily of cytoplasmic tyrosine kinases: structure, regulation, and function. Semin. Immunol., 7, 237-246.
43. Rawlings, D.J., Scharenberg, A.M., Park, H., Wahl, M.I., Lin, S., Kato, R.M., Fluckiger, A.-C., Witte, O.N. and Kinet, J.-P. (1996) Activation of BTK by a phosphorylation mechanism initiated by SRC family kinases. Science, 271, 822-825.
44. Rhee, S.G. and Bae, Y.S. (1997) Regulation of phosphoinositide-specific phospholipase C isozymes. J. Biol. Chem., 272, 15045-15048.
45. Rigley, K.P., Harnett, M.M., Phillips, R.J. and Klaus, G.G.B. (1989) Analysis of signaling via surface immunoglobulin receptors on B cells from CBA/N mice. Eur. J. Immunol., 19, 2081-2086.
46. Salim, K. et al (1996) Distinct specificity in the recognition of phosphoinositides by the pleckstrin homology domains of dynamin and Bruton's tyrosine kinase. EMBO J., 15, 6241-6250.
47. Scharenberg, A.M. and Kinet, J.-P. (1996) The emerging field of receptor-mediated inhibitory signaling: SHP or SHIP? Cell, 87, 961-964.
48. Scharenberg, A.M., Lin, S., Cuenod, B., Yamamura, H. and Kinet, J.-P. (1995) Reconstitution of interactions between tyrosine kinases and the high affinity IgE receptor which are controlled by receptor clustering. EMBO J., 14, 3385-3394.
49. Serunian, L.A., Auger, K.R. and Cantley, L.C. (1991) Identification and quantification of polyphosphoinositides produced in response to platelet-derived growth factor stimulation. Methods Enzymol., 198, 78-87.
50. Stephens, L.R., Hughes, K.T. and Irvine, R.F. (1991) Pathway of phosphatidylinositol(3.4, 5)-trisphosphate synthesis in activated neutrophils. Nature, 351, 33-39.
51. Stokoe, D., Stephens, L.R., Copeland, T., Gaffney, P.R.J., Reese, C.B., Painter, G.F., Holmes, A.B., Mcormick, F. and Hawkins, P.T. (1997) Dual role of phosphatidylinositol-3, 4, 5-trisphosphate in the activation of protein kinase B. Science, 267, 567-569.
52. Takahashi-Tezuka, M., Hibi, M., Fujitani, Y., Fukada, T., Yamaguchi, T. and Hirano, T. (1997) Tec tyrosine kinase links the cytokine receptors to PI-3 kinase probably through JAK. Oncogene, 14, 2273-2282.
53. Takata, M. and Kurosaki, T. (1996) A role for Bruton's tyrosine kinase in B cell antigen receptor-mediated activation of phospholipase C-γ2. J. Exp. Med., 184, 31-40.
54. 2+ mobilization through distinct pathways. EMBO J., 13, 1341-1349.
55. Toker, A. and Cantley, L.C. (1997) Signalling through the lipid products of phosphoinositide-3-OH kinase. Nature, 387, 673-676.
56. Tsukada, S., Simon, M.I., Witte, O.N. and Katz, A. (1994) Binding of the βγ subunits of heterotrimeric G-proteins to the PH domain of Bruton's tyrosine kinase. Proc. Natl Acad. Sci. USA, 91, 11256-11260.
57. Uckun, F.M., Waddick, K.G., Mahajan, S., Jun, X., Takata, M., Bolen, J. and Kurosaki, T. (1996) BTK as a mediator of radiation-induced apoptosis in DT-40 lymphoma B cells. Science, 273, 1096-1100.
58. Vanhaesebroeck, B., Leevers, S.J., Panayotou, G. and Waterfield, M.D. (1997) Phosphoinositide 3-kinases: a conserved family of signal transducers. Trends Biochem. Sci., 22, 267-272.
59. Wan, Y., Bence, K., Hata, A., Kurosaki, T., Veillette, A. and Huang, X.Y. (1997) Genetic evidence for a tyrosine kinase cascade preceding the mitogen-activated protein kinase cascade in vertebrate G protein signaling. J. Biol. Chem., 272, 17209-17215.
60. YangW. and Desiderio, S. (1997) BAP-135, a target for Bruton's tyrosine kinase in response to B cell receptor engagement. Proc. Natl Acad. Sci. USA, 94, 604-609.
61. Yao, L., Kawakami, Y. and Kawakami, T. (1994) The pleckstrin homology domain of Bruton tyrosine kinase interacts with protein kinase C. Proc. Natl Acad. Sci. USA, 91, 9175-9179.